Tuberc Respir Dis.  2016 Apr;79(2):58-69. 10.4046/trd.2016.79.2.58.

Epidemiology of Lung Cancer in Korea: Recent Trends

• Park JY
• Jang SH

• KMID: 2320767
• DOI: http://doi.org/10.4046/trd.2016.79.2.58

Abstract

Lung cancer causes the most cancer deaths in Korea. Although the smoking rate has begun to decrease, the prevalence of lung cancer is still increasing. We reviewed the national lung cancer registry data and the data published about lung cancer in Korea. In 2012, the crude incidence rate of lung cancer was 43.9 per 100,000. The age-standardized mortality rate of lung cancer was 19.8 per 100,000. The 5-year relative survival rate for lung cancer was 11.3% from 1993 to 1995 and increased to 21.9% in the period from 2008 to 2012. Lung cancer occurring in never-smokers was estimated to increase in Korea. Adenocarcinoma is steadily increasing in both women and men and has replaced squamous cell carcinoma as the most common type of lung cancer in Korea. In patients with adenocarcinoma, the frequency of EGFR mutations was 43% (range, 20%-56%), while that of the EMK4-ALK gene was less than 5%.

Keyword

Lung Neoplasms; Korea; Incidence; Mortality; Survival; Prevalence

MeSH Terms

Adenocarcinoma
Carcinoma, Squamous Cell
Epidemiology*
Female
Humans
Incidence
Korea*
Lung Neoplasms*
Lung*
Male
Mortality
Prevalence
Smoke
Smoking
Survival Rate
Smoke

Figure

• 

  Figure 1 Trends in crude rates and age-standardized lung cancer incidence rates in the Korean population from 1999 to 2012. (A) Overall. (B) Men. (C) Women. Source: Annual report of cancer statistics in Korea in 2012 (Korea Central Cancer Registry, 2015)2.

• 

  Figure 2 Trends in histological type of lung cancer and age-standardized smoking rates in Korea. (A) Overall. (B) Men. (C) Women. Source: Annual report of cancer statistics in Korea in 2012 (Korea Central Cancer Registry, 2015)2; Korean Statistical Information Service (Statistics Korea, 2015)11.

• 

  Figure 3 Mortality trends for lung cancer in the Korean population. (A) Number of deaths. (B) Crude mortality rates. (C) Age-standardized mortality rates. Source: Korean Statistical Information Service (Statistics Korea, 2015)11.

Reference

1. Global Burden of Disease Cancer Collaboration. Fitzmaurice C, Dicker D, Pain A, Hamavid H, Moradi-Lakeh M, et al. The global burden of cancer 2013. JAMA Oncol. 2015; 1:505–527.

2. Korea Central Cancer Registry. Annual report of cancer statistics in Korea in 2012 [Internet]. Goyang: National Cancer Information Center;2015. cited 2015 Mar 31. Available from: http://www.cancer.go.kr/.

3. In KH, Kwon YS, Oh IJ, Kim KS, Jung MH, Lee KH, et al. Lung cancer patients who are asymptomatic at diagnosis show favorable prognosis: a Korean Lung Cancer Registry Study. Lung Cancer. 2009; 64:232–237.

4. Park JH, Lee KS, Choi KS. Burden of cancer in Korea during 2000-2020. Cancer Epidemiol. 2013; 37:353–359.

5. World DataBank. World development indicators [Internet]. Washington, DC: The World Bank Group;2015. cited 2015 Nov 11. Available from: http://databank.worldbank.org/ddp/home.dohttp://databank.worldbank.org/ddp/home.do.

6. Planchard D, Besse B. Lung cancer in never-smokers. Eur Respir J. 2015; 45:1214–1217.

7. Wakelee HA, Chang ET, Gomez SL, Keegan TH, Feskanich D, Clarke CA, et al. Lung cancer incidence in never smokers. J Clin Oncol. 2007; 25:472–478.

8. Kang H, Park CW, Kim W, Song SY, Na KJ, Jeong JU, et al. Never-smoker lung cancer is increasing. J Lung Cancer. 2012; 11:89–93.

9. Couraud S, Souquet PJ, Paris C, Do P, Doubre H, Pichon E, et al. BioCAST/IFCT-1002: epidemiological and molecular features of lung cancer in never-smokers. Eur Respir J. 2015; 45:1403–1414.

10. Ha SY, Choi SJ, Cho JH, Choi HJ, Lee J, Jung K, et al. Lung cancer in never-smoker Asian females is driven by oncogenic mutations, most often involving EGFR. Oncotarget. 2015; 6:5465–5474.

11. Korean Statistical Information Service. Statistics Korea [Internet]. Daejeon: Statistics Korea;2015. cited 2015 Sep 23. Available from: http://kosis.kr/.

12. Gloeckler Ries LA, Reichman ME, Lewis DR, Hankey BF, Edwards BK. Cancer survival and incidence from the Surveillance, Epidemiology, and End Results (SEER) program. Oncologist. 2003; 8:541–552.

13. Lortet-Tieulent J, Soerjomataram I, Ferlay J, Rutherford M, Weiderpass E, Bray F. International trends in lung cancer incidence by histological subtype: adenocarcinoma stabilizing in men but still increasing in women. Lung Cancer. 2014; 84:13–22.

14. Zhou C. Lung cancer molecular epidemiology in China: recent trends. Transl Lung Cancer Res. 2014; 3:270–279.

15. Toyoda Y, Nakayama T, Ioka A, Tsukuma H. Trends in lung cancer incidence by histological type in Osaka, Japan. Jpn J Clin Oncol. 2008; 38:534–539.

16. Gray N. The consequences of the unregulated cigarette. Tob Control. 2006; 15:405–408.

17. Marugame T, Sobue T, Nakayama T, Suzuki T, Kuniyoshi H, Sunagawa K, et al. Filter cigarette smoking and lung cancer risk: a hospital-based case: control study in Japan. Br J Cancer. 2004; 90:646–651.

18. Dela Cruz CS, Tanoue LT, Matthay RA. Lung cancer: epidemiology, etiology, and prevention. Clin Chest Med. 2011; 32:605–644.

19. Kenfield SA, Wei EK, Stampfer MJ, Rosner BA, Colditz GA. Comparison of aspects of smoking among the four histological types of lung cancer. Tob Control. 2008; 17:198–204.

20. Ahn MJ, Lee J, Park YH, Ahn JS, Ziogas A, Zell JA, et al. Korean ethnicity as compared with white ethnicity is an independent favorable prognostic factor for overall survival in non-small cell lung cancer before and after the oral epidermal growth factor receptor tyrosine kinase inhibitor era. J Thorac Oncol. 2010; 5:1185–1196.

21. Jung KW, Won YJ, Kong HJ, Oh CM, Cho H, Lee DH, et al. Cancer statistics in Korea: incidence, mortality, survival, and prevalence in 2012. Cancer Res Treat. 2015; 47:127–141.

22. Allemani C, Weir HK, Carreira H, Harewood R, Spika D, Wang XS, et al. Global surveillance of cancer survival 1995-2009: analysis of individual data for 25,676,887 patients from 279 population-based registries in 67 countries (CONCORD-2). Lancet. 2015; 385:977–1010.

23. Alberg AJ, Brock MV, Ford JG, Samet JM, Spivack SD. Epidemiology of lung cancer: diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest. 2013; 143:5 Suppl. e1S–e29S.

24. Howlader N, Noone AM, Krapcho M, Garshell J, Miller D, Altekruse SF, et al. SEER cancer statistics review, 1975-2012. Bethesda: National Cancer Institute;2015.

25. Donington JS, Colson YL. Sex and gender differences in non-small cell lung cancer. Semin Thorac Cardiovasc Surg. 2011; 23:137–145.

26. Wang LE, Yin M, Dong Q, Stewart DJ, Merriman KW, Amos CI, et al. DNA repair capacity in peripheral lymphocytes predicts survival of patients with non-small-cell lung cancer treated with first-line platinum-based chemotherapy. J Clin Oncol. 2011; 29:4121–4128.

27. Soo RA, Loh M, Mok TS, Ou SH, Cho BC, Yeo WL, et al. Ethnic differences in survival outcome in patients with advanced stage non-small cell lung cancer: results of a meta-analysis of randomized controlled trials. J Thorac Oncol. 2011; 6:1030–1038.

28. Ou SH, Ziogas A, Zell JA. Asian ethnicity is a favorable prognostic factor for overall survival in non-small cell lung cancer (NSCLC) and is independent of smoking status. J Thorac Oncol. 2009; 4:1083–1093.

29. Gandara DR, Kawaguchi T, Crowley J, Moon J, Furuse K, Kawahara M, et al. Japanese-US common-arm analysis of paclitaxel plus carboplatin in advanced non-small-cell lung cancer: a model for assessing population-related pharmacogenomics. J Clin Oncol. 2009; 27:3540–3546.

30. Yun YH, Lim MK, Jung KW, Bae JM, Park SM, Shin SA, et al. Relative and absolute risks of cigarette smoking on major histologic types of lung cancer in Korean men. Cancer Epidemiol Biomarkers Prev. 2005; 14:2125–2130.

31. Lee PN, Forey BA, Coombs KJ. Systematic review with meta-analysis of the epidemiological evidence in the 1900s relating smoking to lung cancer. BMC Cancer. 2012; 12:385.

32. Janjigian YY, McDonnell K, Kris MG, Shen R, Sima CS, Bach PB, et al. Pack-years of cigarette smoking as a prognostic factor in patients with stage IIIB/IV nonsmall cell lung cancer. Cancer. 2010; 116:670–675.

33. Kogure Y, Ando M, Saka H, Chiba Y, Yamamoto N, Asami K, et al. Histology and smoking status predict survival of patients with advanced non-small-cell lung cancer. Results of West Japan Oncology Group (WJOG) Study 3906L. J Thorac Oncol. 2013; 8:753–758.

34. Yano T, Haro A, Shikada Y, Maruyama R, Maehara Y. Non-small cell lung cancer in never smokers as a representative 'non-smoking-associated lung cancer': epidemiology and clinical features. Int J Clin Oncol. 2011; 16:287–293.

35. Couraud S, Zalcman G, Milleron B, Morin F, Souquet PJ. Lung cancer in never smokers: a review. Eur J Cancer. 2012; 48:1299–1311.

36. Bae JM. Modifiable risk factors of lung cancer in neversmoker women. Epidemiol Health. 2015; Oct. 29. [Epub]. DOI: 10.4178/epih/e2015047.

37. Hackshaw AK, Law MR, Wald NJ. The accumulated evidence on lung cancer and environmental tobacco smoke. BMJ. 1997; 315:980–988.

38. Zhong L, Goldberg MS, Parent ME, Hanley JA. Exposure to environmental tobacco smoke and the risk of lung cancer: a meta-analysis. Lung Cancer. 2000; 27:3–18.

39. Nordquist LT, Simon GR, Cantor A, Alberts WM, Bepler G. Improved survival in never-smokers vs current smokers with primary adenocarcinoma of the lung. Chest. 2004; 126:347–351.

40. Quoix E, Monnet I, Scheid P, Hamadouche A, Chouaid C, Massard G, et al. Management and outcome of French elderly patients with lung cancer: an IFCT survey. Rev Mal Respir. 2010; 27:421–430.

41. Toh CK, Gao F, Lim WT, Leong SS, Fong KW, Yap SP, et al. Never-smokers with lung cancer: epidemiologic evidence of a distinct disease entity. J Clin Oncol. 2006; 24:2245–2251.

42. Kawaguchi T, Takada M, Kubo A, Matsumura A, Fukai S, Tamura A, et al. Gender, histology, and time of diagnosis are important factors for prognosis: analysis of 1499 never-smokers with advanced non-small cell lung cancer in Japan. J Thorac Oncol. 2010; 5:1011–1017.

43. Straif K, Cohen A, Samet J. Air pollution and cancer [Internet]. Lyon: International Agency for Research on Cancer;2013. cited 2015 Nov 11. Available from: http://www.iarc.fr/en/publications/books/sp161/AirPollutionandCancer161.pdf.

44. Gallus S, Negri E, Boffetta P, McLaughlin JK, Bosetti C, La Vecchia C. European studies on long-term exposure to ambient particulate matter and lung cancer. Eur J Cancer Prev. 2008; 17:191–194.

45. Katanoda K, Sobue T, Satoh H, Tajima K, Suzuki T, Nakatsuka H, et al. An association between long-term exposure to ambient air pollution and mortality from lung cancer and respiratory diseases in Japan. J Epidemiol. 2011; 21:132–143.

46. Hwang SS, Lee JH, Jung GW, Lim JH, Kwon HJ. Spatial analysis of air pollution and lung cancer incidence and mortality in 7 metropolitan cities in Korea. J Prev Med Public Health. 2007; 40:233–238.

47. Sung JH, Cho SH, Kang DH, Yoo KY. Lung cancer, chronic obstructive pulmonary disease and air pollution. Korean J Prev Med. 1997; 30:585–598.

48. Desai MA, Mehta S, Smith KR. Indoor smoke from solid fuels: assessing the environmental burden of disease at national and local levels [Internet]. Geneva: World Health Organization;2004. cited 2015 Nov 11. Available from: http://www.who.int/quantifying_ehimpacts/publications/en/Indoorsmoke.pdf.

49. Lissowska J, Bardin-Mikolajczak A, Fletcher T, Zaridze D, Szeszenia-Dabrowska N, Rudnai P, et al. Lung cancer and indoor pollution from heating and cooking with solid fuels: the IARC international multicentre case-control study in Eastern/Central Europe and the United Kingdom. Am J Epidemiol. 2005; 162:326–333.

50. Zhao Y, Wang S, Aunan K, Seip HM, Hao J. Air pollution and lung cancer risks in China: a meta-analysis. Sci Total Environ. 2006; 366:500–513.

51. Yu IT, Chiu YL, Au JS, Wong TW, Tang JL. Dose-response relationship between cooking fumes exposures and lung cancer among Chinese nonsmoking women. Cancer Res. 2006; 66:4961–4967.

52. Kim C, Gao YT, Xiang YB, Barone-Adesi F, Zhang Y, Hosgood HD, et al. Home kitchen ventilation, cooking fuels, and lung cancer risk in a prospective cohort of never smoking women in Shanghai, China. Int J Cancer. 2015; 136:632–638.

53. Peek RM Jr, Mohla S, DuBois RN. Inflammation in the genesis and perpetuation of cancer: summary and recommendations from a national cancer institute-sponsored meeting. Cancer Res. 2005; 65:8583–8586.

54. Brenner DR, Boffetta P, Duell EJ, Bickeboller H, Rosenberger A, McCormack V, et al. Previous lung diseases and lung cancer risk: a pooled analysis from the International Lung Cancer Consortium. Am J Epidemiol. 2012; 176:573–585.

55. Denholm R, Schuz J, Straif K, Stucker I, Jockel KH, Brenner DR, et al. Is previous respiratory disease a risk factor for lung cancer? Am J Respir Crit Care Med. 2014; 190:549–559.

56. Antoniou KM, Tomassetti S, Tsitoura E, Vancheri C. Idiopathic pulmonary fibrosis and lung cancer: a clinical and pathogenesis update. Curr Opin Pulm Med. 2015; 21:626–633.

57. Kwak N, Park CM, Lee J, Park YS, Lee SM, Yim JJ, et al. Lung cancer risk among patients with combined pulmonary fibrosis and emphysema. Respir Med. 2014; 108:524–530.

58. Lee T, Park JY, Lee HY, Cho YJ, Yoon HI, Lee JH, et al. Lung cancer in patients with idiopathic pulmonary fibrosis: clinical characteristics and impact on survival. Respir Med. 2014; 108:1549–1555.

59. Cancer Genome Atlas Research Network. Comprehensive molecular profiling of lung adenocarcinoma. Nature. 2014; 511:543–550.

60. Midha A, Dearden S, McCormack R. EGFR mutation incidence in non-small-cell lung cancer of adenocarcinoma histology: a systematic review and global map by ethnicity (mutMapII). Am J Cancer Res. 2015; 5:2892–2911.

61. Park JY, Jang SH, Kim HJ, Park YB, Kwon JH, Song HH, et al. Predicting the treatment response using a direct sequencing method for EGFR in non-squamous, non-small cell lung cancer. Korean J Med. 2011; 81:611–622.

62. Jang TW, Oak CH, Chang HK, Suo SJ, Jung MH. EGFR and KRAS mutations in patients with adenocarcinoma of the lung. Korean J Intern Med. 2009; 24:48–54.

63. Kim HJ, Lee KY, Kim YC, Kim KS, Lee SY, Jang TW, et al. Detection and comparison of peptide nucleic acid-mediated real-time polymerase chain reaction clamping and direct gene sequencing for epidermal growth factor receptor mutations in patients with non-small cell lung cancer. Lung Cancer. 2012; 75:321–325.

64. Min KW, Kim WS, Jang SJ, Choi YD, Chang S, Jung SH, et al. Comparison of EGFR mutation detection between the tissue and cytology using direct sequencing, pyrosequencing and peptide nucleic acid clamping in lung adenocarcinoma: Korean multicentre study. QJM. 2016; 109:167–173.

65. Sun PL, Seol H, Lee HJ, Yoo SB, Kim H, Xu X, et al. High incidence of EGFR mutations in Korean men smokers with no intratumoral heterogeneity of lung adenocarcinomas: correlation with histologic subtypes, EGFR/TTF-1 expressions, and clinical features. J Thorac Oncol. 2012; 7:323–330.

66. Shaw AT, Yeap BY, Mino-Kenudson M, Digumarthy SR, Costa DB, Heist RS, et al. Clinical features and outcome of patients with non-small-cell lung cancer who harbor EML4-ALK. J Clin Oncol. 2009; 27:4247–4253.

67. Kang HJ, Lim HJ, Park JS, Cho YJ, Yoon HI, Chung JH, et al. Comparison of clinical characteristics between patients with ALK-positive and EGFR-positive lung adenocarcinoma. Respir Med. 2014; 108:388–394.

68. Chia PL, Mitchell P, Dobrovic A, John T. Prevalence and natural history of ALK positive non-small-cell lung cancer and the clinical impact of targeted therapy with ALK inhibitors. Clin Epidemiol. 2014; 6:423–432.

69. Soda M, Choi YL, Enomoto M, Takada S, Yamashita Y, Ishikawa S, et al. Identification of the transforming EML4-ALK fusion gene in non-small-cell lung cancer. Nature. 2007; 448:561–566.

70. Koivunen JP, Mermel C, Zejnullahu K, Murphy C, Lifshits E, Holmes AJ, et al. EML4-ALK fusion gene and efficacy of an ALK kinase inhibitor in lung cancer. Clin Cancer Res. 2008; 14:4275–4283.

71. Gainor JF, Shaw AT. Novel targets in non-small cell lung cancer: ROS1 and RET fusions. Oncologist. 2013; 18:865–875.

72. Yoo SS, Jin G, Jung HJ, Hong MJ, Choi JE, Jeon HS, et al. RET fusion genes in Korean non-small cell lung cancer. J Korean Med Sci. 2013; 28:1555–1558.

73. Bae EY, Lee SY, Kang BK, Lee EJ, Choi YY, Kang HG, et al. Replication of results of genome-wide association studies on lung cancer susceptibility loci in a Korean population. Respirology. 2012; 17:699–706.

74. Ahn MJ, Won HH, Lee J, Lee ST, Sun JM, Park YH, et al. The 18p11.22 locus is associated with never smoker non-small cell lung cancer susceptibility in Korean populations. Hum Genet. 2012; 131:365–372.